Introduction

Swimming either in public or private pools is a sport generally enjoyed by all age groups particularly during warm seasons of the year. However, the sharing of swimming pools has been reported to lead to disease outbreaks.¹ This is despite the fact that there are guidelines that had been set by the World Health Organization (WHO) with the purpose of minimizing the risk of illnesses and infections originating from them. There have been reports of the contamination of swimming facilities by bacteria and other microbes, some of which have led to diseases of the eye, ear, skin, and digestive system.^23.-4 Other reported diseases are infections associated with upper respiratory tract in immunocompromised patients⁵ with the WHO¹ attributing such outbreaks to poor techniques at disinfection and sometimes the complete lack of disinfecting of these pools. Also, a report by Centers for Disease Control and Prevention (CDC) had pointed to an increase in the number of recreational water illnesses (RWIs) outbreaks for over a period of 2 decades.⁶ This report attributed to the fact that chlorine treatment of swimming pools did not result in the killing of germs. It is stipulated that Protozoa parasites such as Cryptosporidium are capable of surviving for days in well-maintained pools with reported cases of diarrhea outbreaks increasing from 3411 cases in the year 2004 to 10 500 in the year 2008.⁷ In addition to these, bacteria of Pseudomonas species are reported to be well adapted to surviving in a wide range of recreational water facilities despite having been disinfected. In a recent assessment of bacteria isolated from community showers before and after chlorination, it was reported that pseudomonal species were more chlorine-resistant than other bacteria species.⁸ This report is contrary to the earlier views of Papadopoulou et al,⁹ who stipulated that swimming pool–related disease outbreaks could be reduced if these pools are well managed. There are, however, other reports of antimicrobial resistance by bacteria isolated from swimming pools against antiseptics and disinfectants, thus pointing to a public health problem that needs to be monitored carefully.¹⁰

Wide ranges of bacteria have been associated with both chlorine-treated and chlorine-free public and private swimming pools. Earlier research¹¹ found that bacteria from chlorinated water were more resistant to disinfectants than were those from un-chlorinated waters. Subsequently, many other research investigations have demonstrated chlorine-resistant bacteria in consumable water and water sources in general.^12,13 All these reports highlight the potential health problems posed by waterborne bacteria that are difficult to eradicate through conventional means of disinfecting and particularly so as drug-resistant genes are easily transferrable. Among the list of such bacteria are Escherichia coli, Staphylococcus aureus, Pseudomonas aeruginosa, Klebsiella species, among others.⁹ Also, some of these encountered bacteria isolates such as Klebsiella pneumonia and P aeruginosa exhibited multidrug resistance (MDR) against tested antibiotics.¹⁴ Reasons given for such MDR by the researchers was that either the guidelines set by WHO aimed at minimizing the spread of infections in swimming pools were not being kept or that waterborne bacteria associated with recreational swimming pools had devised strategies to withstand eradication through disinfecting. Thus, the threat posed by MDR bacteria carrying drug-resistant genes cannot therefore be overlooked as they can be transferred, creating more public health problems.

Generally, the importance of hygiene in the prevention of bacterial infections cannot be overemphasized. In clinical settings, there are reports of pathogens which have shown decreased susceptibility to antiseptics.^1516.-17 Although such bacterial resistance against disinfectants in clinical settings are a major cause for nosocomial infections, their transference to either private of public swimming pools will be cause for public health concern.¹⁸ Also, as diseases resulting from infections caused by S aureus, E coli, Clostridium perfringens, and Enterococcus faecalis, which had been isolated from different depths of pools by Saberianpour et al,⁵ there is the possibility of transference of clinical-resistant genes to bacteria in communities through swimming pools. Humans continue to make water contact with bacteria-contaminated swimming pools even in an era when there is a global pandemic resulting from MDR bacteria pathogen. This makes it necessary for a more frequent and continuous monitoring of bacteria isolates from all types of swimming pools. The present investigation looks into characterization and antimicrobial susceptibility of Gram-negative bacteria isolates associated with some public and private swimming facilities in the region of the study.

Materials and Methods

Results

The following Gram-negative bacteria isolates were encountered in the study: Pseudomonas aeruginosa, Pseudomonas stutzeri, Pseudomonas mendocina, Klebsiella pneumoniae, Acinetobacter baumannii complex, Acinetobacter lwoffii, E coli, Aeromonas sobria, Aeromonas hydrophila/caviae, Leclercia adecarboxylata, Enterobacter asburiae, Enterobacter cloacae complex, and Cronobacter sakazakii (formerly Enterobacter sakazakii). The percentage frequency of occurrence of these isolates is shown in Figure 1. The figure shows K pneumoniae to be the most encountered bacteria constituting of 50% of the isolates. The cumulative frequency of occurrence of all pseudomonal species was 57.14%, of which P aeruginosa made up 43% of the isolates. A comparison of the types of bacteria isolates from the private and public swimming facilities is shown in Table 1. There were 13 Gram-negative bacteria isolates encountered, and they are shown in Table 1. Ten (77%) of these were isolates from private pools, whereas 5 (39%) isolates were isolated from the public pools. All K pneumoniae isolates were from private pools, whereas P aeruginosa was encountered from both public and privately used pool. Also, Acinetobacter species encountered in the study were isolated from private pools as shown in Table 1.

Figure 1.

Frequency distribution of encountered bacteria isolates from public and private water recreation pools.

Table 1.

Comparison of bacteria isolates between private and public recreational water facilities.

An overall antimicrobial resistance against tested antibiotic was as follows: cefazolin 81%, cefalexin 76.2%, ampicillin 67%, cefuroxime axetil 57%, cefuroxime 57%, amoxicillin/clavulanic acid 38%, ampicillin/sulbactam 33%, and nitrofurantoin 24%. There was a 14.3% resistance exhibited against tigecycline and meropenem each by the isolate, whereas 4.46% of were found to be resistant to imipenem and the results are shown Figure 2. The results on the minimum inhibitory concentration values to the antibiotics are shown in Table 2, whereas results of susceptibility of the isolates against the tested antibiotics are shown in Figure 3. Of the listed 16 antimicrobials used in the investigation, P aeruginosa were resistant to 13 (81%), Acinetobacter species were resistant to 12 (75%), whereas K pneumoniae exhibited resistance to 9 (56%) of the antimicrobials. The figure also shows that resistance to the carbapenems and tigecycline was seen only among Pseudomonas and Acinetobacter species. Also, depending on the depth of pool of bacteria collection, there was no specific pattern of microbial susceptibility against the tested antibiotics as is shown in the results presented in Table 3.

Figure 2.

Showing percentage antimicrobial resistance against the tested antibiotics.

Table 2.

Minimum inhibitory concentration for selected antibiotics used in treatment of Gram-negative bacteria.

Figure 3.

Comparison of percentage resistance by Gram-negative isolates against antibiotics of choice in treatment.

Table 3.

Comparison of antimicrobial susceptibility of bacteria isolates in relation to the source of isolation.

Discussion

The public health risk for the transmission of bacterial infections through swimming pools is highlighted by the results of this study. This problem is more emphasized with private swimming pools in the region of the present investigation than those shared public recreation pools. Similar findings had been reported by researchers^19,24 and in different regions of the world.⁹ The findings on the isolation of K pneumoniae, P aeruginosa, Acinetobacter species, E coli, among other bacteria species are similar to those of Mansoorian et al,²⁵ who reported that the most important bacteria isolates in their research were P aeruginosa, K pneumoniae, Pseudomonas species, E coli, and species of Acinetobacter. However, although they had encountered these bacteria on the surfaces of both private and public pools, the findings in the present report showed P aeruginosa and other pseudomonal species to be the most commonly encountered species in both the public and private pools. Differences could be attributed to regional methods used for the disinfecting of the pools as well as possible difference in the response circulation bacteria clones the disinfecting agents. Also worth noting, however, is that there were more types of bacteria species isolated from the private swimming pools in the present investigation than were those isolated from the public ones.

That all the K pneumoniae in this study were from private pools is a public health risk as these pools are usually visited by holiday makers who rent the farm houses where the pools are located. This is consistent with the findings of Papadopoulou et al,⁹ who reported the isolation of K pneumoniae from in-door swimming pool, from where they had also encountered the highest percentage of multi-antibiotic-resistant bacteria. Although healthy people do not usually get K pneumoniae infections, the bacterium could, however, constitute a health problem to users particularly when it gains entry into the respiratory system or in the case of users who are immunocompromised, where the bacterium could cause pneumonia.

Generally, therefore, the high frequency of bacteria isolation from private pools suggests the probability of non-compliance to WHO recommendations for the disinfection swimming pools. Thus, the differences in disinfecting techniques between owners of private pools and those of the public pools could explain why there were such variations in the number of isolated bacteria species as seen from the results in the region of the present investigation. However, that P aeruginosa and other species of Pseudomonas were isolated from both the private and public swimming pools in this investigation, could be attributed to the ubiquitous nature of the bacterium at being able to survive in moist environments as well as resist antiseptics and antimicrobial.²⁶ Reports, on pool contamination by pseudomonal species, that vary as similar to the present findings are those of other researchers in other regions of the world.^5,14 However, contrary to the results of the present report are those of other researchers.¹⁹ Tirodimos et al¹⁴ found the prevalence of P aeruginosa to be low in their investigation as well as their isolates displaying a low antibiotic resistant pattern. They stipulated that the low antimicrobial resistance by P aeruginosa isolates in their study was indicative of area of low antibiotic usage.¹⁴ The 43% frequency of occurrence for P aeruginosa shown in the results of this investigation is similar to that of 42% earlier reported.¹⁹ Differences in findings could be attributed to regional variation as well as a number of other possible contributory factors. There is the possibility of non-compliance with the chlorination standards set by the WHO in some cases as the private pools in this report were more contaminated than those of the public ones. The maintenance of the public pools appears to be better than what is likely the case of those own privately. Alternatively, there could be the probability of resistance to chlorine as had been reported by researchers from other regions of the world.¹⁴ However, literature is silent on such findings in the region of this study.

In terms of the susceptibility to antimicrobial drugs, the 81% resistance seen with P aeruginosa isolates is high. In our earlier report on P aeruginosa clinical isolate from the region of the present investigation, a growing resistance to anti-pseudomonal drugs was observed and reported with the caution to a close monitoring of this bacterium in the this south-eastern region of Saudi Arabia.²⁷ Tirodimos et al¹⁴ had also found the P aeruginosa isolates in their research to be highly resistant to antimicrobials and attributed this to be due to the fact that the bacterium is naturally resistant to many antibiotics including those of first and second cephalosporins, first-generation fluoroquinolones among a wide range of other antimicrobials. However, that these bacteria isolates are environmentally isolated samples could constitute of a public health concern that needs monitoring.

There is a view that high antimicrobial resistance by environmental bacteria isolates could be as a result of uncontrolled disposal of antibiotics into the environment or that the disposal of hospital waste has created environmental bacteria carrying clones exhibiting high antimicrobial resistance.²⁴ The report indicated the development of adaptive process engaged by bacteria which alter colony traits that help increase their virulence and resistance to antimicrobials in the environment. There is the probability that the encountered pseudomonal species are carrying antimicrobial-resistant clones of clinical origin. This more so as the region of this study is known generally for bacteria strains that are highly resistant to antibiotics. It is also worth noting that resistance to the carbapenems and tigecycline which was associated with A baumannii, other Acinetobacter species, and P aeruginosa could be pointing to the carrying of resistant clinical clones by these environmental isolates. Acinetobacter, an opportunistic pathogen affecting immunocompromised patients, has received much attention by researchers in the region of the present investigation in recent years.²⁸ The study, therefore, shows the potential health risk associated with use of these water recreational facilities and that K pneumoniae and P aeruginosa are the most frequently encountered isolates suggests that there is a need for monitoring.